Understanding the responses of marine phytoplankton to experimental warming

Abstract

Understanding how marine phytoplankton will fare in response to the expected increases in ocean temperature over the next century is crucial for improving their inclusion in models of ocean biogeochemistry. Marine phytoplankton plays an essential role for the global carbon cycle, accounting for approximately 50% of global primary production, and provides the base of all aquatic food webs. There is currently poor understanding of what sets the limits of thermal tolerance and how quickly different species of phytoplankton can adapt to changes in environmental temperature. Furthermore, models that have previously factored for the response of phytoplankton to warming have tended to generalise their inclusion by applying the Eppley coefficient to make predictions about future ocean productivity; this is an across-species characterisation of the thermal sensitivity of phytoplankton growth rates, which assumes a monotonic, exponential, increase in maximal growth rates with temperature. To enhance our understanding of the responses of marine phytoplankton to warming we first investigated the limits of thermal tolerance, as well as the thermal performance of both photosynthesis and respiration rates, for an array of phytoplankton taxa, representing key functional groups, including: cyanobacteria, diatoms, coccolithophores, dinoflagellates and chlorophytes. We identify, qualitatively, that the limits of thermal tolerance are likely to be underpinned by the thermal performance of metabolism, whereby across all taxa respiration was more temperature dependent, and generally had a higher optimal temperature, than photosynthesis. Next, using the understanding of thermal tolerance at the species level we estimated an across-species temperature dependence of maximal growth rates that was lower than the within-species average, supporting the “partial compensation” mechanism of thermal adaptation and highlighting that the canonical Eppley coefficient is likely to under or overestimate the temperature dependence in ocean regions where particular species, or phylogenetic groups, may dominate. With this finding we were also able to associate greater thermal tolerance with covariance of other ecologically important physiological and morphological traits, highlighting that the likely restructuring of phytoplankton communities in response to warming will have strong implications for ecosystem function and biogeochemical cycles. Lastly, we investigated the pace and magnitude of thermal adaptation to a stressful supra-optimal temperature across three very different but ecologically important phytoplankton species. We found that across the three taxa there was clear variance in the rate and magnitude of thermal adaptation, with the least complex and smallest of the three taxa showing the fastest rates of thermal adaptation and the greatest improvement in thermal tolerance. Underpinning thermal adaptation across the taxa were clear metabolic adjustments, likely to be associated with overcoming the constraints of carbon allocation to growth due to the differing thermal sensitivities of photosynthesis and respiration. We conclude that each of the main findings from this research can help improve the inclusion of marine phytoplankton in models of ocean biogeochemistry and as part of wider Earth systems models, thereby aiding predictions of the likely reorganisation of phytoplankton communities and the impact of warming on the critical ecosystem services and biogeochemical cycles that phytoplankton mediate.